Phylum-Wide Analysis of SSU rDNA Reveals Deep Phylogenetic Relationships among Nematodes and Accelerated Evolution toward Crown Clades

TLDR

Inference of nematode evolutionary relationships is hampered by conserved morphology, frequent homoplasy, and scarce phylum‑wide molecular data. The study aims to investigate the origin of nematode radiation and the phylogenetic relationships among distantly related species. It analyzes 339 nearly full‑length small‑subunit rDNA sequences from a diverse range of nematodes. Bayesian inference revealed a 12‑clade backbone, with the basal clade dominated by Enoplia and Triplonchida near the common ancestor, while crown clades 8–12 show accelerated substitution rates linked to parasitic lifestyles or short generation times, enabling DNA‑barcode species identification.

Abstract

Inference of evolutionary relationships between nematodes is severely hampered by their conserved morphology, the high frequency of homoplasy, and the scarcity of phylum-wide molecular data. To study the origin of nematode radiation and to unravel the phylogenetic relationships between distantly related species, 339 nearly full-length small-subunit rDNA sequences were analyzed from a diverse range of nematodes. Bayesian inference revealed a backbone comprising 12 consecutive dichotomies that subdivided the phylum Nematoda into 12 clades. The most basal clade is dominated by the subclass Enoplia, and members of the order Triplonchida occupy positions most close to the common ancestor of the nematodes. Crown Clades 8–12, a group formerly indicated as “Secernentea” that includes Caenorhabditis elegans and virtually all major plant and animal parasites, show significantly higher nucleotide substitution rates than the more basal Clades 1–7. Accelerated substitution rates are associated with parasitic lifestyles (Clades 8 and 12) or short generation times (Clades 9–11). The relatively high substitution rates in the distal clades resulted in numerous autapomorphies that allow in most cases DNA barcode–based species identification. Teratocephalus, a genus comprising terrestrial bacterivores, was shown to be most close to the starting point of Secernentean radiation. Notably, fungal feeding nematodes were exclusively found basal to or as sister taxon next to the 3 groups of plant parasitic nematodes, namely, Trichodoridae, Longidoridae, and Tylenchomorpha. The exclusive common presence of fungivorous and plant parasitic nematodes supports a long-standing hypothesis that states that plant parasitic nematodes arose from fungivorous ancestors.